Identifying Barriers and Facilitators to Care for Infants with Bronchopulmonary Dysplasia After NICU Discharge: A Prospective Study of Parents and Clinical Stakeholders

Objective Understand barriers and facilitators to follow-up care for infants with bronchopulmonary dysplasia (BPD). Methods Qualitative study of parents and clinical stakeholders caring for infants with BPD. The interview guide was developed by a mother of a former 23-week preterm infant, neonatologist, pulmonologist, nurse, and qualitative researcher. Purposive sampling obtained a heterogenous sociodemographic and professional cohort. Subjects discussed their experience with BPD, barriers to care, caregiver quality of life and health education. Interviews were audio-recorded, transcribed and coded. Thematic analysis was used. Results Eighteen parents and 20 stakeholders completed interviews. Family-level themes included pragmatic barriers like transportation being multi-faceted; and caregiving demands straining mental health. System-level themes included caregiver education needing to balance process needs with future trajectories; and integration of primary care, specialty care, and community supports. Conclusions Individual and system barriers impact follow-up for infants with BPD. This conceptual framework can be used to measure and improve care.


Background
Infants born extremely preterm are at high risk of developing bronchopulmonary dysplasia (BPD).(1)(2)(3)(4)(5)(6)(7) In the United States, 10,000 to 15,000 infants develop BPD each year.(8)BPD has major implications for young children and families as they transition home from neonatal intensive care; 70% of infants with BPD experience post-prematurity respiratory disease by 1 year of age.(9)(10)(11) Compared to other preterm infants, infants with BPD experience longer NICU stays and more re-hospitalizations.(12)(13)(14) Respiratory symptoms such as wheezing can persist throughout childhood leading to more medication use, outpatient and emergency care.(15)(16)(17)(18)(19)(20) Durable medical equipment leads to frequent interactions with specialist healthcare providers, home nursing and equipment companies.Although it has been shown that these complex health needs negatively impact parent health-related quality of life, it is not known how healthcare supports may serve as barriers or facilitators for families caring for infants with BPD as they transition home from the NICU.(15-20)A deeper understanding of child and family experiences with post-discharge healthcare utilization for infants with BPD would inform better discharge practices for infants with this complex condition.
Multidisciplinary supports after NICU discharge are intended to improve outcomes for infants; however, specialty care can only improve outcomes if families can access supports.Unfortunately, families of infants with BPD may face signi cant barriers to care.Prematurity disproportionately impacts families experiencing socioeconomic disadvantage, who in turn experience barriers to accessing the outpatient follow-up care that could improve health outcomes.(21)(22)(23)(24) Socioeconomic and racial disparities in NICU care have been increasingly highlighted, and likely contribute to disparities in parent discharge preparation for high-needs infants.(25)(26)(27)(28)(29) Health systems vary widely in clinic sta ng and care coordination.(21,(30)(31)(32)(33) Research to understand the nuances to these potential barriers to care for infants with BPD would help inform a conceptual framework for measurement, research and improvement.
The goal of this study was to better understand barriers and facilitators to care among stakeholders and parents of infants of BPD, in order to understand how to improve discharge preparation and follow-up care for infants with BPD.

Recruitment and Study Population
This was a qualitative study using semi-structured interviews of parents and clinical stakeholders caring for infants with BPD, following consolidated criteria for reporting qualitative research.(34) Parents and clinical stakeholders were identi ed for potential participation by members of the research team with clinical or professional knowledge of potential participants (MH, MM, SD, JL).Purposive sampling was used to obtain a heterogenous sample across sociodemographic characteristics for parents and across professional roles for stakeholders.Parents were recruited in person from the NICU, BPD pediatric pulmonology clinic and developmental follow-up clinic, with clinical team members introducing the interviewer to families.Parent-infant dyads who met the following inclusion criteria were invited to participate in the study: 1) infant born < 32 weeks; 2) diagnosed with BPD de ned by receipt of respiratory support at 36 weeks' corrected age in the NICU; 3) at least one English speaking parent; 4) no tracheostomy (due to the different level of complexity and team involvement for that patient population).
Stakeholders were invited by email.Eligibility included being either a healthcare provider caring for infants with BPD in the inpatient or outpatient clinical setting, or a staff member experienced with preterm infants and their families transitioning from hospital to home, such as a social worker, case manager, or community service professional (e.g., Special Supplemental Nutrition Program for Women, Infants, and Children professionals).Subjects were recruited until thematic saturation.The study was reviewed and approved as exempt by the institutional review board of the Medical College of Wisconsin.All participants provided verbal consent to participate.Interviews were offered in person, via phone or computer; 2 interviews were completed in person and the rest were completed over the phone with audio recording.Parents signed a HIPAA waiver for viewing the infant health record and received a $25 gift card for participation.

Interview Content
Interviews were conducted individually by a research assistant trained in qualitative interview methods.
The interviewer is a doctoral student and mother of a former 23-week preterm infant, working in collaboration with a neonatologist, pediatric pulmonologist, nurse, and qualitative research expert to construct the interview guide.Stakeholders and parents were told about the members of the interview team and the background of the interviewer.Interview guides followed a similar format for parents and stakeholders (Table 2).For parents, content areas included 1) parent's personal history leading up to their child's preterm birth; 2) the child's health symptoms over time; 3) perspectives on health services including gaps in care, barriers, facilitators, and resources; 4) quality of life including social support, physical and mental health.For stakeholders, we asked about 1) professional roles related to caring for preterm infants with BPD; 2) perspectives on important symptoms and issues for patients with BPD (for clinical stakeholders); 3) perspectives on key supports for infants with BPD, including challenges to accessing care and providing condition-speci c health education; 4) issues regarding family quality of life and social support.The interview guide was tested with a sample of parents and stakeholders before beginning the study.all transcripts and codes to identify and discuss any potential discrepancies.Coded interviews were analyzed using thematic analysis to identify emerging themes.(37)A grounded theory approach was used to examine concepts and themes within the data and develop an explanatory framework of barriers and facilitators to care as identi ed by stakeholders and parents of infants with BPD.(36, 38)

Results
A total of 25 parents were approached for participation; 25 agreed to participate, and 18 completed interviews with the remaining 7 not completed due to scheduling di culty and thematic saturation.A total of 22 stakeholders were approached for participation; 20 completed interviews.Parents represented a range of education, income, race and ethnicity.Stakeholders represented a range of specialty and primary care, social work, care coordination, and community services (Table 1).Each interview occurred only once.Interviews ranged from 25-60 minutes to complete.
Interviews of parents and stakeholders identi ed four primary themes (Fig. 1).Family-level themes included multifaceted social needs and family functioning affecting navigation of NICU and postdischarge care.System-level themes included caregiver education needing to balance tangible process needs and broader expectations, and communication and coordination of services.
The multifaceted nature of social needs exacerbates barriers to screening and service referrals Pragmatic barriers to attendance in the NICU and post-discharge appointments were commonly described by both parents and stakeholders (Table 3).Transportation was a major barrier to attending follow-up appointments and was described by both parents and stakeholders as multi-faceted.Transportation barriers included individual or family barriers such as not having a car, not having money to afford gas, and having to arrange childcare for siblings in order to attend clinics; they also included system barriers such as unreliable transportation services and appointment in exibility in the case of late arrivals.Stakeholders felt that responding to even a speci c barrier like transportation was often nuanced.Inpatient-based stakeholders noted that resource referrals bene tted from in-person communication to properly assess and refer to resources, whereas outpatient teams generally described involvement after a pattern of inability to make appointments.Primary care teams felt that transportation may be more of a barrier to specialty services further from home than to their clinics.

Emotional toll of caregiving
"He got discharged at, around 42 weeks so he was weeks of a newborn baby but like a super, super, super premature baby.I came home and we really didn't have anyone in the house.We didn't take him places.So, I think our social aspect of friends and family has taken a big hit for us.Which kind of trickles down mentally for everyone because we're not living our lifestyles like we did a year ago, with the kids being able to have friends over; we've said no to a lot of social gatherings just for, you know, exposures."(Parent 13) "Emotionally and just physically having to do the stuff that came with her conditions like changing her oxygen tank, cleaning out her oxygen converter, making sure if it's sticky, get cleaned …took an emotional toll on me.Just by seeing and having it there and knowing she's not a normal baby."(Parent 11) "I think it is de nitely for some families it's hard, and it's stressful, 'cause it's a lot to handle for these families, especially if they need oxygen or other types of equipment, and it can be scary… I think there's de nitely a lot of anxiety with these babies that the families have.And they're de nitely hyper aware of certain symptoms.Or some families, I can tell they have problems sleeping through the night because they always feel like they have to go check on their baby to make sure that their baby's breathing."(Stakeholder 1) Most parents felt that the NICU and clinics do well in addressing needs such as transportation.While receiving resources was helpful in reducing barriers, some parents described wanting to be aware of resources sooner.Stakeholders agreed that there was a lack of awareness of available resources, which may be due in part to limitations in systematic screening for social needs.Reasons provided for limited systematic screening included changing needs over time which may not be uncovered during initial screenings, a perceived overwhelming degree of needs, and insu cient supportive resources.
Family functioning: Competing health and caregiving demands strain family and mental health Parents commonly expressed challenges balancing the competing life demands of employment and family in addition to the caregiving needs of an infant with a complex health condition (Table 3).Speci c barriers included not having childcare to attend appointments, the regimented daily requirements for infants with medical equipment along with needs of other siblings, and the desire to reduce infectious exposures limiting the availability of help.When parents needed to alternate time in the NICU with other family or job demands, this exacerbated family functioning stress after discharge because other family members' lack of training in the NICU meant there were fewer prepared caregivers to help with an infant's needs at home.Some parents described not working after NICU discharge to be able to solely care for their infant, or having opposite shifts of their signi cant other or family, as a solution to sharing care needs.Parents also discussed the family and mental health strain caused by social isolation and competing demands for such a long time.Some parents expressed trauma related to their infant's care needs, including guilt of preterm delivery, being back in the hospital, seeing that the baby "isn't normal," and being cognitively but not emotionally prepared for the workload required.Facilitators to family functioning included exibility to limit work, ability and expectations to share sibling care, and prior experiences dealing with healthcare.More modi able facilitators included trust in nurses or healthcare providers to gain support, networking opportunities with other families, connection to resources to reduce nancial barriers, and ability to seek mental health support.
Stakeholders similarly identi ed that families were challenged with competing life demands such as balancing work and childcare responsibilities, and the strain placed on individuals and family relationships.Some stakeholders expressed that fear of the healthcare system after their experiences with pregnancy and the NICU can lead to a need to get away from the hospital and potentially avoid subsequent healthcare system exposure, but can also lead to fear of leaving the hospital and hypervigilance about certain symptoms.Clinical stakeholders expressed the importance of family functioning in supporting child health, but most acknowledged that they do not universally ask about these issues due to available time and resources.From a stakeholder perspective, facilitators to improving family function included better resources to support both pragmatic needs and psychosocial support.

Caregiver education needs to balance tangible process needs and broader expectations
Parents overall described receiving excellent instruction focused on equipment management and infant care (Table 4).Facilitators to caregiver self-e cacy included home nurses, teaching materials, being present in the NICU for more preparation time, and reassurance from supportive providers.Themes in educational gaps included anxiety about the learning curve; many parents felt that their how-to instruction was good, but that the mental preparation was nerve-wracking.Many parents noted the difference between observing skills demonstrated in the NICU and taking primary responsibility at home.
A frequent request was to offer more second-caregiver education; many mothers reported being the only person trained to use equipment, do feeding, and give medications, which then caused di culty after discharge because of competing needs and delay in other caregivers being able to provide support."Some parents are like, 'Well, they won't make it to pulmonology to gure out their oxygen situation.Can this baby be weaned off of oxygen?'They need pulse oximetry for that to be done, right?And that's something that I can't do as a pediatrician.I've had parents just taking off.They'll just be like, 'Oh, well, let's see how they do at home.'And they'll just wean off their kid's own oxygen or no longer have an oxygen order.And so the kid is just done with their oxygen, right?…What do you do as a pediatrician?"(Stakeholder 11)

Parent quotes Stakeholder quotes
Opportunities and limitations of support services "I knew that from the home care agency we had a nurse coming to the house, and so I felt supported... I'll be honest.At rst, I didn't think I was gonna need the home care nurse, but I was so grateful to have her, because she would help me pick up on things, and not maybe feel so overwhelmed."(Parent 1) "In-home therapy has helped tremendously because when she was starting she doesn't even know she has legs, seriously, and now she's walking and they recommended the prosthesis for her feet and everything."(Parent 5) "How-to videos [are] on our website… [in a] third to fth grade [reading level] so that the voice-over for that how-to video would be accessible to a family member.So if they're having a problem with the suction machine and they wanna troubleshoot it or how do you apply an oximeter probe, that they could go and have that reinforcement to them 24/7.And it's there free on our website to anybody in the world, whether they're our patient or not.That is something that we've been able to provide just based on a commitment to safe care in the home."(Stakeholder 18) "Some families do not engage in all this and there are systemic barriers… where families fear that if you have someone coming into your home on a week-to-week or month-to-month basis, even if it is designed as a supportive presence, there is a deep-rooted fear for some of these families that it will be used against them in the future, that if they acknowledge a need, that it could be used against them, whether it's with Child Protection Services or other consequences."( Stakeholders identi ed several discrete educational needs.These included process needs such as understanding equipment, handling medication re lls, and knowing who to call after discharge; acute care education such as mitigating viral exposures and actions prior to seeking emergency care; and preventive care needs such as the role of specialty follow-up.Speci c to infants with BPD who have had ongoing intermittent desaturations in the NICU for weeks to months, a gap was also noted in understanding the importance of appropriate oxygen saturations.Expected trajectory was identi ed as a gap; examples included expectations for school, exercise limitation, duration of respiratory support, and when childcare outside the home could be safer.Stakeholders emphasized that health literacy and stress were major barriers to educating families around infant diagnosis and care needs.

Care coordination and communication: important and constrained by system limitations
Parents thought that post-discharge appointments was not a challenge in itself; however, clustering appointments together was di cult given limited appointment availability (Table 4).Parents also identi ed communication between teams as a system barrier to obtaining care; examples included communication between specialists and pediatrician, or between multiple teams and the family, as to clear delineation of roles and the "why" for each visit.Some parents felt that their primary care provider was reluctant to interfere with specialist recommendations so as not to provide con icting information, and as a result the families were not sure of their pediatrician's comfort with their child's medical needs.
Parents identi ed the need to advocate for their child across system gaps such as lack of follow-through with scheduling between teams or resources; they identi ed their own background or education as a facilitator for those with a background in healthcare, and they identi ed healthcare providers' insensitivity at times to family challenges as a barrier to being able to advocate strongly.Those who participated in care coordination programs found it helpful for scheduling and team communication.
Stakeholders also highlighted that specialty provider availability can pose barriers to care.The use of care coordination services was seen as a potential facilitator to help alleviate the challenges of multiple appointments, but limitations included that families may not appreciate that bene t immediately.Another issue that stakeholders highlighted was con icting recommendations between providers leading to confusion; examples included recommendations on nutrition issues or who to call with acute respiratory symptoms.
Some constructs were present across multiple individual and system themes (Fig. 1).Social determinants of health crossed all levels of barriers to care, in that nancial barriers limited access to in-person communication to enable education of primary and secondary caregivers, which perpetuated problems with extended family support and abilities to advocate for better care coordination.Health literacy was commonly identi ed by stakeholders as an educational barrier, whereas parents were more likely to describe it indirectly as a barrier or facilitator in advocating for coordination of care.Complexity of needs including medications, equipment or frequent appointments impacted need for education and care coordination, but also was mentioned as a contributor to family and mental health strain.

Discussion
The goal of this study was to identify barriers and facilitators to care among stakeholders and parents of infants of BPD, in order to understand how to improve discharge preparation and follow-up care speci c to this condition.Our main ndings were: 1) the multi-faceted nature of social needs exacerbates barriers to screening and resource referrals; 2) competing health and caregiving demands strain family functioning and mental health; 3) caregiver education needs to balance tangible process needs and expected trajectories within the context of stress and variable health literacy; 4) care coordination opportunities are both important and constrained by system limitations in pediatric subspecialty care.
Given the lengthy NICU stays, and frequent outpatient appointments required of infants with BPD, it is not surprising that pragmatic barriers such as transportation were a major theme impacting access to care.
Both parents and clinical stakeholders recognized that supporting needs such as transportation were multi-faceted, and both parents and clinical stakeholders recognized the limitations of community resources in supporting these needs.In response to these barriers and limitations, parents more frequently expressed desires to be provided with earlier, ongoing screening to increase their awareness of resources.Stakeholders were more likely to prefer in-person introductions to establish rapport and understand a family's needs in more detail; after that introduction, subsequent resource referrals were more likely to occur after a pattern of nonattendance or an explicit request.From a system standpoint, depending on in-person interaction to identify a need for assistance with getting to in-person appointments can delay or prevent understanding of families' needs and getting them connected to resources.Systematic screening for social determinants of health is increasingly recognized as an important way to improve health outcomes.(39)(40)(41)(42)(43) The application of systematic screening for resource needs has been more widely demonstrated in outpatient settings; adaptations to the inpatient setting are emerging more recently.(40,41) To support infants with BPD preparing for complex discharge home from the NICU, it may be helpful to consider both inpatient and outpatient scenarios to help families envision their upcoming needs and arm themselves with appropriate resources.
Both parents and stakeholders recognized the family and mental health strain resulting from competing caregiving demands.While some aspects of social support are not modi able by a health care team, it was encouraging to observe that parents identi ed several actionable ways to increase family capacity.Identifying ways to increase educational offerings such that additional caregivers do not need to be trained solely by the parent who was able to be at the bedside could be an important facilitator of postdischarge family capacity, since the differential in caregiver comfort causes frequently reported family strain.Videos or multi-media offerings could assist family caregivers who are not able to be present for all hospital and clinic-based education.Anticipatory support for mental health including the trauma of preterm birth and emotions surrounding a baby who requires signi cant post-discharge medical supports are important topics to address before and after NICU discharge.Most NICUs have limited social work and psychology resources to assist families, but this limitation is likely even more pronounced in the outpatient setting.Systematic outpatient psychosocial support as part of NICU follow-up is critical especially for fragile infants such as those with BPD, since parents commonly describe that nothing could prepare them for the emotional toll of home caregiving despite their cognitive preparation.
While both parents and stakeholders generally identi ed good education to help teach processes related to their infants' care needs, they all also agreed on the gap in education on expected needs of a child with BPD over time.Even for infants with multiple outpatient clinical and community support resources, the weeks and months spent in the NICU before going home may be the majority of time available for direct hands-on family caregiver education.This time is spent learning infant care, which can be overwhelming even before adding the complex needs of an infant with BPD.Strategies to enhance anticipatory guidance about life after the NICU might include earlier identi cation of equipment and medication needs, and more proactive meetings with relevant outpatient specialists to understand early childhood needs.It should be noted that some themes emerged in duality, such that it was di cult to disentangle family functioning from educational themes that pose barriers to meeting the needs of families with a child with BPD.Ongoing psychosocial support and multi-media educational offerings are crucial to working effectively within the context of stress, rotating work schedules, and variable health literacy that limit the ability to process information.
Even in the context of perceived high quality specialty care, families and stakeholders noted system limitations to care coordination.Dedicated care coordination teams are helpful facilitators to complex care, but do not always enroll infants with BPD going home from the NICU.NICU-speci c transition-home programs have been shown to be effective in reducing health care expenditures and readmissions but have not become widespread across NICUs.(44)(45)(46)(47) Our ndings were consistent with this literature.
Parents who did not receive care coordination agreed that care coordination would improve barriers, and those who did receive care coordination felt it made attending appointments easier.However, even in the presence of a care coordination team, outpatient pediatric subspecialty availability can limit the ability to streamline appointments; multidisciplinary clinics may improve this system gap.Parents also perceived primary care physicians to have variably active involvement with their child's specialty needs.Consensus recommendations for outpatient management of BPD do not currently highlight roles for the primary care provider versus specialist care or a recommended schedule for pulmonology follow-up, leading to a lack of clarity on best practices to guide care coordination.
Strengths of this study include an interview guide designed to elicit multiple levels of potential barriers to care, parallel interviews between both parents and clinical stakeholders, intentional sampling strategy to recruit a diverse range of participants, and analysis integrating the perspectives of a parent of a preterm infant, nurse, and physician.Our ndings provide detail that can be used to understand opportunities for system interventions to improve care for infants with BPD.We acknowledge several limitations.The study was conducted at one health system, although we did explicitly recruit parents of infants cared for at multiple NICUs.Although our qualitative strategy allows for a detailed understanding of perspectives, and we interviewed until reaching thematic saturation, the study cohort may not be representative of the whole population.Although the interviewer self-identi ed as a parent of a preterm infant and not a direct healthcare provider, there may be some desirability bias affecting parent willingness to acknowledge barriers within the healthcare system.Although the interview guide was constructed by multidisciplinary members of the research team, the interviewer's life experience as a parent of preterm infant with BPD may have led to researcher bias.Additionally, parents who are unaware of community resources or healthcare system differences may not be able to fully identify potential barriers to obtaining care for their infant.Clinical stakeholders employed by our healthcare system, although anonymous, may also experience desirability bias in discussing potential system limitations to care.They also may differ in their sense of frequency of barriers to care compared to families, as has been demonstrated previously. (48)

Conclusion
In this qualitative study of parents and stakeholders, we identi ed discrete yet inter-related domains of barriers and facilitators to follow-up care for infants with BPD after the NICU.These include pragmatic social barriers, caregiver strain impacting family functioning, family function impacting educational needs, and opportunities and limits to care coordination for pediatric specialty care.Despite different perspectives, families and stakeholders converged on several themes that could improve care for infants Conceptual framework of barriers to care for infants with bronchopulmonary dysplasia after discharge.
Themes and examples were identi ed by thematic analysis of interviews with both parents and clinical stakeholders.

Table 2
Sample interview prompts for stakeholders and parents.

Table 3
Representative parent and stakeholder quotes on family-level barriers and facilitators to care here?Do we need gas cards or … a cab to come and get us….See, we didn't know all of this.We could have been using this resource and …kept the car at home, and rode up here if they woulda' signed it up like that.Butthey didn't say none of that until the last minute."(Parent 12) "I think the other thing we always fear in screening… is what are we gonna do to help them once we have this information?Because we're often inundated with needs… A lot of the social determinants of health are hard for us to screen for because everybody needs help here."(Stakeholder 7) Complexity of needs "The transportation [isn't] always reliable either… because sometimes something gets messed up on there, so we must call, reschedule your appointment or you just might get to your appointment late or something like that, and then they're not able to see you and you have to reschedule.Driving yourself [is] not always ideal because the gas prices.. before, they were kind of outrageous."(Parent 21) When you're able to assess the family, you nd out that there is a lot more complexity behind it… Perhaps it's

Table 4
Representative parent and stakeholder quotes on system-level barriers and facilitators to care After they are healthy enough to get home and they see, 'Oh, they're healthy enough to be off of oxygen,' then the question always is like, 'What's next?' …I have that conversation of, 'You know what?You know, I fully expect your child to be running around on the basketball courts or soccer elds at, you know, at kindergarten, rst grade.And if they're not, if they're the kids that sit down on the bench and it's because they can't breathe, don't assume that's because of[BPD].You need to come back and let us know and also let the pediatricians know that too.' We've had a couple families that said, 'Oh, we just thought it was because they were born premature.'And they're 12 years old, and they've limited themselves.They're deconditioned.They're wheezing.We could've made your quality of life and your health better if we just had known.(Stakeholder 2) "Any of those barriers in getting to us, you only have to deal with one hurdle instead of three consecutive days.And these families have a lot of appointments.I don't know how they do it.I'llbe honest with you.I'm a collegeeducated, well-organized person, and the thought of sometimes they're coming three days a week to our institution, that's a lot on anybody."(Stakeholder5)